Characterization of 14-3-3 isoforms expressed in the Echinococcus granulosus pathogenic larval stage

Journal of Proteome Research

Volumn 14, Issue 4, 2015, Pages 1700-1715

  Teichmann, Aline ^a   Vargas, Daiani M ^a   Monteiro, Karina M ^a   Meneghetti, Bruna V ^a   Dutra, Cristine S ^a   Paredes, Rodolfo ^b   Galanti, Norbel ^c   Zaha, Arnaldo ^a   Ferreira, Henrique B ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b UNIVERSIDAD ANDRÉS BELLO   (Chile)

^c UNIVERSITY OF CHILE   (Chile)

Author keywords

14 3 3 proteins; Echinococcus granulosus; host parasite interactions; protein protein interactions

Indexed keywords

CARBOHYDRATE; HELMINTH PROTEIN; HELMINTH RNA; ISOPROTEIN; PROTEIN 14 3 3; RECOMBINANT PROTEIN; BENZHYDRYL DERIVATIVE; EMPAGLIFLOZIN; GLUCOSIDE; LIGAND;

ADULT; AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CROSS REACTION; DIMERIZATION; ECHINOCOCCUS GRANULOSUS; ENZYME PHOSPHORYLATION; GEL ELECTROPHORESIS; HOST PARASITE INTERACTION; HUMAN; IMMUNOBLOTTING; ISOELECTRIC POINT; LARVAL STAGE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METACESTODE; MOLECULAR MODEL; MONOPHYLY; NONHUMAN; PARTICLE SIZE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SEQUENCE ALIGNMENT; ANIMAL; CLUSTER ANALYSIS; ECHINOCOCCOSIS; FLUORESCENT ANTIBODY TECHNIQUE; GENE STRUCTURE; GENETICS; LARVA; MASS SPECTROMETRY; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PARASITOLOGY; PATHOGENICITY;

ECHINOCOCCUS GRANULOSUS; EUKARYOTA;

14-3-3 PROTEINS; AMINO ACID SEQUENCE; ANIMALS; BENZHYDRYL COMPOUNDS; CHROMATOGRAPHY, AFFINITY; CLONING, MOLECULAR; CLUSTER ANALYSIS; ECHINOCOCCOSIS; ECHINOCOCCUS GRANULOSUS; FLUORESCENT ANTIBODY TECHNIQUE; GENE COMPONENTS; GLUCOSIDES; IMMUNOBLOTTING; LARVA; LIGANDS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN INTERACTION MAPPING; PROTEIN ISOFORMS;

EID: 84926506131     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr5010136     Document Type: Article

References (67)

1. Nakao, M.; Lavikainen, A.; Yanagida, T.; Ito, A. Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae) Int. J. Parasitol. 2013, 43, 1017-29
2. Balbinotti, H.; Santos, G. B.; Badaraco, J.; Arend, A. C.; Graichen, D.; Haag, K. L.; Zaha, A. Echinococcus ortleppi (G5) and Echinococcus granulosus sensu stricto (G1) loads in cattle from Southern Brazil Vet Parasitol. 2012, 188, 255-60
3. Alvarez Rojas, C. A.; Romig, T.; Lightowlers, M. W. Echinococcus granulosus sensu lato genotypes infecting humans-review of current knowledge Int. J. Parasitol. 2014, 44, 9-18
4. de la Rue, M. L.; Takano, K.; Brochado, J. F.; Costa, C. V.; Soares, A. G.; Yamano, K.; Yagi, K.; Katoh, Y.; Takahashi, K. Infection of humans and animals with Echinococcus granulosus (G1 and G3 strains) and E. ortleppi in Southern Brazil Vet Parasitol. 2011, 177, 97-103
5. Díaz, A.; Casaravilla, C.; Irigoín, F.; Lin, G.; Previato, J. O.; Ferreira, F. Understanding the laminated layer of larval Echinococcus I: structure Trends Parasitol. 2011, 27, 204-13
6. Siracusano, A.; Riganò, R.; Ortona, E.; Profumo, E.; Margutti, P.; Buttari, B.; Delunardo, F.; Teggi, A. Immunomodulatory mechanisms during Echinococcus granulosus infection Exp. Parasitol. 2008, 119, 483-9
7. Monteiro, K.; de Carvalho, M.; Zaha, A.; Ferreira, H. Proteomic analysis of the Echinococcus granulosus metacestode during infection of its intermediate host Proteomics 2010, 10, 1985-1999
8. Aziz, A.; Zhang, W.; Li, J.; Loukas, A.; McManus, D. P.; Mulvenna, J. Proteomic characterisation of Echinococcus granulosus hydatid cyst fluid from sheep, cattle and humans J. Proteomics 2011, 74, 1560-72
9. Virginio, V. G.; Monteiro, K. M.; Drumond, F.; de Carvalho, M. O.; Vargas, D. M.; Zaha, A.; Ferreira, H. B. Excretory/secretory products from in vitro -cultured Echinococcus granulosus protoscoleces Mol. Biochem. Parasitol. 2012, 183, 15-22
10. Pozuelo Rubio, M.; Geraghty, K. M.; Wong, B. H.; Wood, N. T.; Campbell, D. G.; Morrice, N.; Mackintosh, C. 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking Biochem. J. 2004, 379, 395-408
11. Kjarland, E.; Keen, T. J.; Kleppe, R. Does isoform diversity explain functional differences in the 14-3-3 protein family? Curr. Pharm. Biotechnol. 2006, 7, 217-23
12. Lalle, M.; Camerini, S.; Cecchetti, S.; Sayadi, A.; Crescenzi, M.; Pozio, E. Interaction network of the 14-3-3 protein in the ancient protozoan parasite Giardia duodenalis J. Proteome Res. 2012, 11, 2666-83
13. Bridges, D.; Moorhead, G. 14-3-3 proteins: a number of functions for a numbered protein Sci. STKE 2005, 2005, re10
14. Victor, B.; Kanobana, K.; Gabriël, S.; Polman, K.; Deckers, N.; Dorny, P.; Deelder, A. M.; Palmblad, M. Proteomic analysis of Taenia solium metacestode excretion-secretion proteins Proteomics 2012, 12, 1860-9
15. Zheng, H.; Zhang, W.; Zhang, L.; Zhang, Z.; Li, J.; Lu, G.; Zhu, Y.; Wang, Y.; Huang, Y.; Liu, J.; Kang, H.; Chen, J.; Wang, L.; Chen, A.; Yu, S.; Gao, Z.; Jin, L.; Gu, W.; Wang, Z.; Zhao, L.; Shi, B.; Wen, H.; Lin, R.; Jones, M. K.; Brejova, B.; Vinar, T.; Zhao, G.; McManus, D. P.; Chen, Z.; Zhou, Y.; Wang, S. The genome of the hydatid tapeworm Echinococcus granulosus Nat. Genet. 2013, 45, 1168-75
16. Siles-Lucas, M.; Merli, M.; Gottstein, B. 14-3-3 proteins in Echinococcus: their role and potential as protective antigens Exp. Parasitol. 2008, 119, 516-23
17. Salazar-Anton, F.; Lindh, J. Taenia solium: a two-dimensional western blotting method combined with the use of an EST-library for the identification of immunogenic proteins recognized by sera from neurocysticercosis patients Exp. Parasitol. 2011, 128, 371-6
18. Tsai, I. J.; Zarowiecki, M.; Holroyd, N.; Garciarrubio, A.; Sanchez-Flores, A.; Brooks, K. L.; Tracey, A.; Bobes, R. J.; Fragoso, G.; Sciutto, E.; Aslett, M.; Beasley, H.; Bennett, H. M.; Cai, J.; Camicia, F.; Clark, R.; Cucher, M.; De Silva, N.; Day, T. A.; Deplazes, P.; Estrada, K.; Fernández, C.; Holland, P. W.; Hou, J.; Hu, S.; Huckvale, T.; Hung, S. S.; Kamenetzky, L.; Keane, J. A.; Kiss, F.; Koziol, U.; Lambert, O.; Liu, K.; Luo, X.; Luo, Y.; Macchiaroli, N.; Nichol, S.; Paps, J.; Parkinson, J.; Pouchkina-Stantcheva, N.; Riddiford, N.; Rosenzvit, M.; Salinas, G.; Wasmuth, J. D.; Zamanian, M.; Zheng, Y.; Taenia solium Genome Consortium; Cai, X.; Soberón, X.; Olson, P. D.; Laclette, J. P.; Brehm, K.; Berriman, M. The genomes of four tapeworm species reveal adaptations to parasitism Nature 2013, 496, 57-63
19. Fernández, C.; Gregory, W.; Loke, P.; Maizels, R. Full-length-enriched cDNA libraries from Echinococcus granulosus contain separate populations of oligo-capped and trans-spliced transcripts and a high level of predicted signal peptide sequences Mol. Biochem. Parasitol. 2002, 122, 171-80
20. Siles-Lucas, M.; Nunes, C.; Zaha, A.; Breijo, M. The 14-3-3 protein is secreted by the adult worm of Echinococcus granulosus Parasite Immunol. 2000, 22, 521-8
21. Besemer, J.; Borodovsky, M. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses Nucleic Acids Res. 2005, 33, W451-4
22. Salamov, A. A.; Solovyev, V. V. Ab initio gene finding in Drosophila genomic DNA Genome Res. 2000, 10, 516-22
23. Burge, C. B.; Karlin, S. Finding the genes in genomic DNA Curr. Opin. Struct. Biol. 1998, 8, 346-54
24. Saitou, N.; Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees Mol. Biol. Evol. 1987, 4, 406-25
25. Tamura, K.; Stecher, G.; Peterson, D.; Filipski, A.; Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0 Mol. Biol. Evol. 2013, 30, 2725-9
26. da Fonsêca, M. M.; Zaha, A.; Caffarena, E. R.; Vasconcelos, A. T. Structure-based functional inference of hypothetical proteins from Mycoplasma hyopneumoniae J. Mol. Model. 2012, 18, 1917-25
27. Yang, X.; Lee, W.; Sobott, F.; Papagrigoriou, E.; Robinson, C.; Grossmann, J.; Sundström, M.; Doyle, D.; Elkins, J. Structural basis for protein-protein interactions in the 14-3-3 protein family Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 17237-42
28. Würtele, M.; Jelich-Ottmann, C.; Wittinghofer, A.; Oecking, C. Structural view of a fungal toxin acting on a 14-3-3 regulatory complex EMBO J. 2003, 22, 987-94
29. Takala, H.; Nurminen, E.; Nurmi, S. M.; Aatonen, M.; Strandin, T.; Takatalo, M.; Kiema, T.; Gahmberg, C. G.; Ylänne, J.; Fagerholm, S. C. Beta2 integrin phosphorylation on Thr758 acts as a molecular switch to regulate 14-3-3 and filamin binding Blood 2008, 112, 1853-62
30. Liu, D.; Bienkowska, J.; Petosa, C.; Collier, R. J.; Fu, H.; Liddington, R. Crystal structure of the zeta isoform of the 14-3-3 protein Nature 1995, 376, 191-4
31. Molzan, M.; Weyand, M.; Rose, R.; Ottmann, C. Structural insights of the MLF1/14-3-3 interaction FEBS J. 2012, 279, 563-71
32. Brokx, S. J.; Wernimont, A. K.; Dong, A.; Wasney, G. A.; Lin, Y. H.; Lew, J.; Vedadi, M.; Lee, W. H.; Hui, R. Characterization of 14-3-3 proteins from Cryptosporidium parvum PLoS One 2011, 6, e14827
33. Eswar, N.; Webb, B.; Marti-Renom, M. A.; Madhusudhan, M. S.; Eramian, D.; Shen, M. Y.; Pieper, U.; Sali, A. Comparative protein structure modeling using MODELLER. Current Protocols in Protein Science; Wiley Interscience: Hoboken, NJ, 2007; Chapter 2, Unit 2.9.
34. Lorenzatto, K. R.; Monteiro, K. M.; Paredes, R.; Paludo, G. P.; da Fonsêca, M. M.; Galanti, N.; Zaha, A.; Ferreira, H. B. Fructose-bisphosphate aldolase and enolase from Echinococcus granulosus: genes, expression patterns and protein interactions of two potential moonlighting proteins Gene 2012, 506, 76-84
35. Paredes, R.; Jiménez, V.; Cabrera, G.; Iragüen, D.; Galanti, N. Apoptosis as a possible mechanism of infertility in Echinococcus granulosus hydatid cysts J. Cell. Biochem. 2007, 100, 1200-9
36. Koziol, U.; Krohne, G.; Brehm, K. Anatomy and development of the larval nervous system in Echinococcus multilocularis Front. Zool. 2013, 10, 24
37. Meek, S.; Lane, W.; Piwnica-Worms, H. Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins J. Biol. Chem. 2004, 279, 32046-54
38. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal. Chem. 2002, 74, 5383-92
39. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75, 4646-58
40. Tatusov, R. L.; Fedorova, N. D.; Jackson, J. D.; Jacobs, A. R.; Kiryutin, B.; Koonin, E. V.; Krylov, D. M.; Mazumder, R.; Mekhedov, S. L.; Nikolskaya, A. N.; Rao, B. S.; Smirnov, S.; Sverdlov, A. V.; Vasudevan, S.; Wolf, Y. I.; Yin, J. J.; Natale, D. A. The COG database: an updated version includes eukaryotes BMC Bioinf. 2003, 4, 41
41. Powell, S.; Forslund, K.; Szklarczyk, D.; Trachana, K.; Roth, A.; Huerta-Cepas, J.; Gabaldón, T.; Rattei, T.; Creevey, C.; Kuhn, M.; Jensen, L. J.; von Mering, C.; Bork, P. eggNOG v4.0: nested orthology inference across 3686 organisms Nucleic Acids Res. 2014, 42, D231-9
42. Ferl, R. J.; Manak, M. S.; Reyes, M. F. The 14-3-3s Genome Biol. 2002, 3, reviews3010
43. Benzinger, A.; Popowicz, G.; Joy, J.; Majumdar, S.; Holak, T.; Hermeking, H. The crystal structure of the non-liganded 14-3-3sigma protein: insights into determinants of isoform specific ligand binding and dimerization Cell Res. 2005, 15, 219-27
44. Gardino, A.; Smerdon, S.; Yaffe, M. Structural determinants of 14-3-3 binding specificities and regulation of subcellular localization of 14-3-3-ligand complexes: a comparison of the X-ray crystal structures of all human 14-3-3 isoforms Semin. Cancer Biol. 2006, 16, 173-82
45. Obsil, T.; Obsilova, V. Structural basis of 14-3-3 protein functions Semin. Cell Dev. Biol. 2011, 22, 663-72
46. Andrade, M.; Siles-Lucas, M.; Espinoza, E.; Pérez Arellano, J.; Gottstein, B.; Muro, A. Echinococcus multilocularis laminated-layer components and the E14t 14-3-3 recombinant protein decrease NO production by activated rat macrophages in vitro Nitric Oxide 2004, 10, 150-5
47. Shimada, T.; Fournier, A. E.; Yamagata, K. Neuroprotective function of 14-3-3 proteins in neurodegeneration Biomed. Res. Int. 2013, 2013, 564534
48. Gygi, S. P.; Corthals, G. L.; Zhang, Y.; Rochon, Y.; Aebersold, R. Evaluation of two-dimensional gel electrophoresis-based proteome analysis technology Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 9390-5
49. Chang, I. F.; Curran, A.; Woolsey, R.; Quilici, D.; Cushman, J. C.; Mittler, R.; Harmon, A.; Harper, J. F. Proteomic profiling of tandem affinity purified 14-3-3 protein complexes in Arabidopsis thaliana Proteomics 2009, 9, 2967-85
50. 2+ signalling BMC Cell Biol. 2007, 8, 31
51. Alexander, R. D.; Morris, P. C. A proteomic analysis of 14-3-3 binding proteins from developing barley grains Proteomics 2006, 6, 1886-96
52. Paul, A. L.; Denison, F. C.; Schultz, E. R.; Zupanska, A. K.; Ferl, R. J. 14-3-3 phosphoprotein interaction networks-does isoform diversity present functional interaction specification? Front. Plant Sci. 2012, 3, 190
53. Uhart, M.; Bustos, D. M. Protein intrinsic disorder and network connectivity. The case of 14-3-3 proteins Front. Genet. 2014, 5, 10
54. Swatek, K. N.; Graham, K.; Agrawal, G. K.; Thelen, J. J. The 14-3-3 isoforms chi and epsilon differentially bind client proteins from developing Arabidopsis seed J. Proteome Res. 2011, 10, 4076-87
55. Kleppe, R.; Martinez, A.; Døskeland, S. O.; Haavik, J. The 14-3-3 proteins in regulation of cellular metabolism Semin. Cell Dev. Biol. 2011, 22, 713-9
56. Parkinson, J.; Wasmuth, J. D.; Salinas, G.; Bizarro, C. V.; Sanford, C.; Berriman, M.; Ferreira, H. B.; Zaha, A.; Blaxter, M. L.; Maizels, R. M.; Fernández, C. A transcriptomic analysis of Echinococcus granulosus larval stages: implications for parasite biology and host adaptation PLoS Negl. Trop. Dis. 2012, 6, e1897
57. Chernik, I. S.; Seit-Nebi, A. S.; Marston, S. B.; Gusev, N. B. Small heat shock protein Hsp20 (HspB6) as a partner of 14-3-3gamma Mol. Cell. Biochem. 2007, 295, 9-17
58. Pan, D.; Das, S.; Bera, A. K.; Bandyopadhyay, S.; De, S.; Rana, T.; Das, S. K.; Suryanaryana, V. V.; Deb, J.; Bhattacharya, D. Molecular and biochemical mining of heat-shock and 14-3-3 proteins in drug-induced protoscolices of Echinococcus granulosus and the detection of a candidate gene for anthelmintic resistance J. Helminthol. 2011, 85, 196-203
59. Jin, J.; Smith, F. D.; Stark, C.; Wells, C. D.; Fawcett, J. P.; Kulkarni, S.; Metalnikov, P.; ODonnell, P.; Taylor, P.; Taylor, L.; Zougman, A.; Woodgett, J. R.; Langeberg, L. K.; Scott, J. D.; Pawson, T. Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization Curr. Biol. 2004, 14, 1436-50
60. Grimm, E.; Portugal, R.; de Oliveira Neto, M.; Martins, N.; Polikarpov, I.; Zaha, A.; Ferreira, H. Structural analysis of an Echinococcus granulosus actin-fragmenting protein by small-angle X-ray scattering studies and molecular modeling Biophys. J. 2006, 90, 3216-23
61. Zhou, Q.; Kee, Y. S.; Poirier, C. C.; Jelinek, C.; Osborne, J.; Divi, S.; Surcel, A.; Will, M. E.; Eggert, U. S.; Müller-Taubenberger, A.; Iglesias, P. A.; Cotter, R. J.; Robinson, D. N. 14-3-3 coordinates microtubules, Rac, and myosin II to control cell mechanics and cytokinesis Curr. Biol. 2010, 20, 1881-9
62. Gardino, A. K.; Yaffe, M. B. 14-3-3 proteins as signaling integration points for cell cycle control and apoptosis Semin. Cell Dev. Biol. 2011, 22, 688-95
63. Smith, A. J.; Daut, J.; Schwappach, B. Membrane proteins as 14-3-3 clients in functional regulation and intracellular transport Physiology 2011, 26, 181-91
64. Dang, Z.; Yagi, K.; Oku, Y.; Kouguchi, H.; Kajino, K.; Watanabe, J.; Matsumoto, J.; Nakao, R.; Wakaguri, H.; Toyoda, A.; Sugimoto, C. Evaluation of Echinococcus multilocularis tetraspanins as vaccine candidates against primary alveolar echinococcosis Vaccine 2009, 27, 7339-45
65. Katoh, Y.; Kouguchi, H.; Matsumoto, J.; Goto, A.; Suzuki, T.; Oku, Y.; Yagi, K. Characterization of emY162 encoding an immunogenic protein cloned from an adult worm-specific cDNA library of Echinococcus multilocularis Biochim. Biophys. Acta 2008, 1780, 1-6
66. Perez-Hernandez, D.; Gutiérrez-Vázquez, C.; Jorge, I.; López-Martín, S.; Ursa, A.; Sánchez-Madrid, F.; Vázquez, J.; Yáñez-Mó, M. The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes J. Biol. Chem. 2013, 288, 11649-61
67. Goc, A.; Abdalla, M.; Al-Azayzih, A.; Somanath, P. R. Rac1 activation driven by 14-3-3ζ dimerization promotes prostate cancer cell-matrix interactions, motility and transendothelial migration PLoS One 2012, 7, e40594